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Parental Benefits and Offspring Costs Reflect Parent–Offspring Conflict Over the Age of Fledging Among Songbirds

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Parental Benefits and Offspring Costs Reflect Parent–Offspring Conflict Over the Age of Fledging Among Songbirds Parental benefits and offspring costs reflect parent–offspring conflict over the age of fledging among songbirds Todd M. Jonesa,b,1, Jeffrey D. Brawna, Ian J. Auspreyc, Andrew C. Vitzd, Amanda D. Rodewalde, Douglas W. Raybuckf, Than J. Bovesg, Cameron J. Fissh,i, Darin J. McNeile,i, Scott H. Stolesonj, Jeffery L. Larkini, W. Andrew Coxk, Amy C. Schwarzerk, Noah P. Horsleya, Evalynn M. Trumboa, and Michael P. Warda,b aDepartment of Natural Resources and Environmental Sciences, University of Illinois at Urbana–Champaign, Urbana, IL 61801; bIllinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana–Champaign, Champaign, IL 61801; cFlorida Museum of Natural History and Department of Biology, University of Florida, Gainesville, FL 32611; dWildlife Section, Massachusetts Division of Fisheries and Wildlife, Westborough, MA 01581; eCornell Lab of Ornithology and Department of Natural Resources, Cornell University, Ithaca, NY 14850; fDepartment of Forestry, Wildlife and Fisheries, University of Tennessee, Knoxville, TN 37996; gDepartment of Biological Sciences, Arkansas State University, Jonesboro, AR 72467; hDepartment of Environmental and Forest Biology, State University of New York College of Environmental Science and Forestry, Syracuse, NY 13210; iDepartment of Biology, Indiana University of Pennsylvania, Indiana, PA 15705; jForestry Sciences Laboratory, United States Department of Agriculture, Forest Service Northern Research Station, Irvine, PA 16329; and kFish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Gainesville, FL 32601 Edited by Glenn-Peter Saetre, University of Oslo, Oslo, Norway, and accepted by Editorial Board Member Scott V. Edwards October 6, 2020 (received for review May 7, 2020) Parent–offspring conflict has explained a variety of ecological phe- be regarded as a result of interactions between parents and their nomena across animal taxa, but its role in mediating when song- offspring. Thus, even though offspring may still be dependent on birds fledge remains controversial. Specifically, ecologists have their parents after leaving the nest, the age at which they leave can long debated the influence of songbird parents on the age of depend on the outcome of conflict between parent and offspring fledging: Do parents manipulate offspring into fledging to opti- interests (5). mize their own fitness or do offspring choose when to leave? To In birds, research has shown that the age of fledging (nest provide greater insight into parent–offspring conflict over fledg- – leaving) is primarily associated with nest mortality risk (6 10), but ECOLOGY ing age in songbirds, we compared nesting and postfledging sur- for many taxa, there is compelling evidence that this timing is also vival rates across 18 species from eight studies in the continental mediated by parent–offspring conflict (summarized in ref. 3). One United States. For 12 species (67%), we found that fledging tran- exception to this pattern, however, is in songbirds, where the role sitions offspring from comparatively safe nesting environments to of parent–offspring conflict remains understudied, unclear, and more dangerous postfledging ones, resulting in a postfledging controversial (2). Studies on fledging in songbirds have centered bottleneck. This raises an important question: as past research shows that offspring would benefit—improve postfledging survival—by around a debate over two hypotheses: 1) the parental manipulation staying in the nest longer: Why then do they fledge so early? Our hypothesis (PMH), in which parents and offspring are in conflict findings suggest that parents manipulate offspring into fledging early over the optimal age of fledging and parents initiate fledging by for their own benefit, but at the cost of survival for each individual manipulating offspring (11); and 2) the nestling choice or threshold offspring, reflecting parent–offspring conflict. Early fledging incurred, on average, a 13.6% postfledging survival cost for each individual Significance offspring, but parents benefitted through a 14.0% increase in the likelihood of raising at least one offspring to independence. These Parent–offspring conflict has explained a variety of ecological parental benefits were uneven across species—driven by an interac- phenomena across animal taxa, but its role in mediating when tion between nest mortality risk and brood size—and predicted the songbirds fledge remains controversial. Our analysis of nesting age of fledging among species. Collectively, our results suggest that and postfledging survival rates within 18 songbird species found parent–offspring conflict and associated parental benefits explain var- that offspring commonly leave safer nesting environments for iation in fledging age among songbird species and why postfledging riskier postfledging ones—known as postfledging bottlenecks. bottlenecks occur. This timing of fledging incurs a cost for offspring survival, but benefits adults by increasing their likelihood of raising at least bottleneck | fledging | parent–offspring conflict | postfledging | songbirds one offspring to independence. Parents therefore appear to manipulate offspring into fledging earlier than expected based onflict between parents and offspring can arise from dis- on the offspring’s ensuing survival prospects. Our results sug- Cagreements over how long periods of parental care should last gest that parent–offspring conflict and associated variation in (sensu, ref. 1). This occurs as extending parental care can enhance parental benefits explain variation in fledging age among offspring fitness, but for adults, the benefits of continuing care are songbird species and why postfledging bottlenecks occur. eventually outweighed by costs to future reproduction and survival (2). Consequently, parent–offspring conflict theory proposes that Author contributions: T.M.J. and M.P.W. designed research; T.M.J., I.J.A., A.C.V., D.W.R., C.J.F., D.J.M., W.A.C., A.C.S., N.P.H., E.M.T., and M.P.W. performed research; T.M.J. ana- the optimal length of parental care differs between parents and lyzed data; and T.M.J., J.D.B., I.J.A., A.C.V., A.D.R., D.W.R., T.J.B., C.J.F., D.J.M., S.H.S., J.L.L., their offspring, with offspring preferring care to continue for a W.A.C., A.C.S., N.P.H., E.M.T., and M.P.W. wrote the paper. longer duration than that preferred by adults (1, 3). The length of The authors declare no competing interest. parental care and optimal timing of independence in animals may This article is a PNAS Direct Submission. G.-P.S. is a guest editor invited by the therefore be reflective of complex behavioral interactions between Editorial Board. parents and offspring as they resolve this evolutionary conflict (4). Published under the PNAS license. Though likely strongest over the optimal timing of offspring in- 1To whom correspondence may be addressed. Email: [email protected]. dependence (1), parent–offspring conflict also mediates the timing This article contains supporting information online at https://www.pnas.org/lookup/suppl/ of other juvenile transitions during the period of parental invest- doi:10.1073/pnas.2008955117/-/DCSupplemental. ment. The age at which animals leave their nests, for instance, can First published November 16, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2008955117 PNAS | December 1, 2020 | vol. 117 | no. 48 | 30539–30546 size hypothesis (NCH), in which parents and offspring are not in Pennsylvania, and Texas. First, we estimated daily survival rates conflict and fledging is initiated by other factors only after offspring for juveniles across the nesting and postfledging period and pass a developmental threshold (11, 12). Perpetuating debate be- compared rates immediately before and after fledging. Second, we tween these hypotheses are studies that focus on the proximate used daily survival rates to derive probabilities of mortality for the factors (parental and offspring behaviors) of fledging. For instance, entire brood and compared brood mortality rates before and after past studies have provided evidence in support of the PMH by fledging. Third, we used daily survival rates to estimate cumulative documenting manipulative behaviors of adults, such as luring off- survival for offspring across the postfledging period. Lastly, we spring with food or reducing their provisioning rates (5, 13, 14), but used nesting and postfledging survival rates to derive estimates of other studies have dismissed such observations as anecdotal or parent–offspring costs and benefits (daily survival rates per indi- misinterpretations of adult behavior (2, 15). Additionally, studies on vidual and per brood) of earlier fledging under scenarios where a these hypotheses have failed to acknowledge an apparent paradox bottleneck does and does not occur. Overall, the goals of our study with respect to fledging. Songbird offspring may be subject to were to use these survival estimates and comparisons to 1) provide postfledging bottlenecks, whereby survival rates immediately fol- evidence to support or refute the NCH and PMH; 2) test for lowing fledging are significantly lower than those in the nest (16), prevalence, severity, and length of postfledging bottlenecks; and 3) with offspring transitioning from a safer nest environment to a more empirically evaluate the influence of parent–offspring conflict on dangerous postfledging one. As experimental and comparative variation in the age at fledging among species by 1) estimating postfledging work shows
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